MBE Advance Access originally published online on April 6, 2005
Molecular Biology and Evolution 2005 22(7):1561-1568; doi:10.1093/molbev/msi145
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Research Article |
Time Dependency of Molecular Rate Estimates and Systematic Overestimation of Recent Divergence Times
* Henry Wellcome Ancient Biomolecules Centre, Department of Zoology, University of Oxford, Oxford, United Kingdom; and Evolutionary Biology Group, Department of Zoology, University of Oxford, Oxford, United Kingdom
E-mail: simon.ho{at}zoo.ox.ac.uk.
Studies of molecular evolutionary rates have yielded a wide range of rate estimates for various genes and taxa. Recent studies based on population-level and pedigree data have produced remarkably high estimates of mutation rate, which strongly contrast with substitution rates inferred in phylogenetic (species-level) studies. Using Bayesian analysis with a relaxed-clock model, we estimated rates for three groups of mitochondrial data: avian protein-coding genes, primate protein-coding genes, and primate d-loop sequences. In all three cases, we found a measurable transition between the high, short-term (<1–2 Myr) mutation rate and the low, long-term substitution rate. The relationship between the age of the calibration and the rate of change can be described by a vertically translated exponential decay curve, which may be used for correcting molecular date estimates. The phylogenetic substitution rates in mitochondria are approximately 0.5% per million years for avian protein-coding sequences and 1.5% per million years for primate protein-coding and d-loop sequences. Further analyses showed that purifying selection offers the most convincing explanation for the observed relationship between the estimated rate and the depth of the calibration. We rule out the possibility that it is a spurious result arising from sequence errors, and find it unlikely that the apparent decline in rates over time is caused by mutational saturation. Using a rate curve estimated from the d-loop data, several dates for last common ancestors were calculated: modern humans and Neandertals (354 ka; 222–705 ka), Neandertals (108 ka; 70–156 ka), and modern humans (76 ka; 47–110 ka). If the rate curve for a particular taxonomic group can be accurately estimated, it can be a useful tool for correcting divergence date estimates by taking the rate decay into account. Our results show that it is invalid to extrapolate molecular rates of change across different evolutionary timescales, which has important consequences for studies of populations, domestication, conservation genetics, and human evolution.
Key Words: mutation rate • substitution rate • rate calibration • purifying selection
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  T. Sota and T. Tanabe Multiple speciation events in an arthropod with divergent evolution in sexual morphology Proc R Soc B, November 4, 2009; (2009) rspb.2009.1822v1. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. I. Peterson and J. Masel Quantitative Prediction of Molecular Clock and Ka/Ks at Short Timescales Mol. Biol. Evol., November 1, 2009; 26(11): 2595 - 2603. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Debruyne and H. N. Poinar Time Dependency of Molecular Rates in Ancient DNA Data Sets, A Sampling Artifact? Syst Biol, July 1, 2009; (2009) syp028v1. [Full Text] [PDF]
|
|
|
|
|
|
S. Subramanian Temporal Trails of Natural Selection in Human Mitogenomes Mol. Biol. Evol., April 1, 2009; 26(4): 715 - 717. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. I. Fraser, R. Nikula, H. G. Spencer, and J. M. Waters From the Cover: Kelp genes reveal effects of subantarctic sea ice during the Last Glacial Maximum PNAS, March 3, 2009; 106(9): 3249 - 3253. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Kawakita and M. Kato Repeated independent evolution of obligate pollination mutualism in the Phyllantheae-Epicephala association Proc R Soc B, February 7, 2009; 276(1656): 417 - 426. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Q. D Atkinson, R. D Gray, and A. J Drummond Bayesian coalescent inference of major human mitochondrial DNA haplogroup expansions in Africa Proc R Soc B, January 22, 2009; 276(1655): 367 - 373. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. M. Henn, C. R. Gignoux, M. W. Feldman, and J. L. Mountain Characterizing the Time Dependency of Human Mitochondrial DNA Mutation Rate Estimates Mol. Biol. Evol., January 1, 2009; 26(1): 217 - 230. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Rodrigo, F. Bertels, J. Heled, R. Noder, H. Shearman, and P. Tsai The perils of plenty: what are we going to do with all these genes? Phil Trans R Soc B, December 27, 2008; 363(1512): 3893 - 3902. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Rosset, R. S. Wells, D. F. Soria-Hernanz, C. Tyler-Smith, A. K. Royyuru, D. M. Behar, and and The Genographic Consortium Maximum-Likelihood Estimation of Site-Specific Mutation Rates in Human Mitochondrial DNA From Partial Phylogenetic Classification Genetics, November 1, 2008; 180(3): 1511 - 1524. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. C Pratt, M. Morgan-Richards, and S. A Trewick Diversification of New Zealand weta (Orthoptera: Ensifera: Anostostomatidae) and their relationships in Australasia Phil Trans R Soc B, October 27, 2008; 363(1508): 3427 - 3437. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. T. Brumfield, L. Liu, D. E. Lum, and S. V. Edwards Comparison of Species Tree Methods for Reconstructing the Phylogeny of Bearded Manakins (Aves: Pipridae, Manacus) from Multilocus Sequence Data Syst Biol, October 1, 2008; 57(5): 719 - 731. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Axelsson, E. Willerslev, M. T. P. Gilbert, and R. Nielsen The Effect of Ancient DNA Damage on Inferences of Demographic Histories Mol. Biol. Evol., October 1, 2008; 25(10): 2181 - 2187. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Y.W Ho, G. Larson, C. J Edwards, T. H Heupink, K. E Lakin, P. W.H Holland, and B. Shapiro Correlating Bayesian date estimates with climatic events and domestication using a bovine case study Biol Lett, August 23, 2008; 4(4): 370 - 374. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. D. Cutter Divergence Times in Caenorhabditis and Drosophila Inferred from Direct Estimates of the Neutral Mutation Rate Mol. Biol. Evol., April 1, 2008; 25(4): 778 - 786. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. P. Burridge, D. Craw, D. Fletcher, and J. M. Waters Geological Dates and Molecular Rates: Fish DNA Sheds Light on Time Dependency Mol. Biol. Evol., April 1, 2008; 25(4): 624 - 633. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. D. Weaver, C. C. Roseman, and C. B. Stringer Close correspondence between quantitative- and molecular-genetic divergence times for Neandertals and modern humans PNAS, March 25, 2008; 105(12): 4645 - 4649. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Koeppel, E. B. Perry, J. Sikorski, D. Krizanc, A. Warner, D. M. Ward, A. P. Rooney, E. Brambilla, N. Connor, R. M. Ratcliff, et al. Identifying the fundamental units of bacterial diversity: A paradigm shift to incorporate ecology into bacterial systematics PNAS, February 19, 2008; 105(7): 2504 - 2509. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Q. D. Atkinson, R. D. Gray, and A. J. Drummond mtDNA Variation Predicts Population Size in Humans and Reveals a Major Southern Asian Chapter in Human Prehistory Mol. Biol. Evol., February 1, 2008; 25(2): 468 - 474. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Craw, C. Burridge, R. Norris, and J. Waters Genetic ages for Quaternary topographic evolution: A new dating tool Geology, January 1, 2008; 36(1): 19 - 22. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Y.W Ho, S.-O. Kolokotronis, and R. G Allaby Elevated substitution rates estimated from ancient DNA sequences Biol Lett, December 22, 2007; 3(6): 702 - 705. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. S. Ort and G. H. Pogson Molecular Population Genetics of the Male and Female Mitochondrial DNA Molecules of the California Sea Mussel, Mytilus californianus Genetics, October 1, 2007; 177(2): 1087 - 1099. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Howell, J. L. Elson, C. Howell, and D. M. Turnbull Relative Rates of Evolution in the Coding and Control Regions of African mtDNAs Mol. Biol. Evol., October 1, 2007; 24(10): 2213 - 2221. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Ogata and J.-M. Claverie Unique genes in giant viruses: Regular substitution pattern and anomalously short size Genome Res., September 1, 2007; 17(9): 1353 - 1361. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. CRAW and J. WATERS Geological and biological evidence for regional drainage reversal during lateral tectonic transport, Marlborough, New Zealand Journal of the Geological Society, July 1, 2007; 164(4): 785 - 793. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Martinkova, R. A McDonald, and J. B Searle Stoats (Mustela erminea) provide evidence of natural overland colonization of Ireland Proc R Soc B, June 7, 2007; 274(1616): 1387 - 1393. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Y. W. Ho, B. Shapiro, M. J. Phillips, A. Cooper, and A. J. Drummond Evidence for Time Dependency of Molecular Rate Estimates Syst Biol, June 1, 2007; 56(3): 515 - 522. [Full Text] [PDF]
|
|
|
|
|
|
S. Y. W. Ho, T. H. Heupink, A. Rambaut, and B. Shapiro Bayesian Estimation of Sequence Damage in Ancient DNA Mol. Biol. Evol., June 1, 2007; 24(6): 1416 - 1422. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. J. Genner, O. Seehausen, D. H. Lunt, D. A. Joyce, P. W. Shaw, G. R. Carvalho, and G. F. Turner Age of Cichlids: New Dates for Ancient Lake Fish Radiations Mol. Biol. Evol., May 1, 2007; 24(5): 1269 - 1282. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. M. Waters, D. L. Rowe, S. Apte, T. M. King, G. P. Wallis, L. Anderson, R. J. Norris, D. Craw, and C. P. Burridge Geological Dates and Molecular Rates: Rapid Divergence of Rivers and Their Biotas Syst Biol, April 1, 2007; 56(2): 271 - 282. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. C. Emerson Alarm Bells for the Molecular Clock? No Support for Ho et al.'s Model of Time-Dependent Molecular Rate Estimates Syst Biol, April 1, 2007; 56(2): 337 - 345. [Full Text] [PDF]
|
|
|
|
 |
|
 J. T. Weir and D. Schluter The Latitudinal Gradient in Recent Speciation and Extinction Rates of Birds and Mammals Science, March 16, 2007; 315(5818): 1574 - 1576. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Goios, L. Pereira, M. Bogue, V. Macaulay, and A. Amorim mtDNA phylogeny and evolution of laboratory mouse strains Genome Res., March 1, 2007; 17(3): 293 - 298. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. C. Spady and E. A. Ostrander Canid genomics: Mapping genes for behavior in the silver fox Genome Res., March 1, 2007; 17(3): 259 - 263. [Full Text] [PDF]
|
|
|
|
|
|
L. A. Zhivotovsky, P. A. Underhill, and M. W. Feldman Difference between Evolutionarily Effective and Germ line Mutation Rate Due to Stochastically Varying Haplogroup Size Mol. Biol. Evol., December 1, 2006; 23(12): 2268 - 2270. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Woodhams Can Deleterious Mutations Explain the Time Dependency of Molecular Rate Estimates? Mol. Biol. Evol., December 1, 2006; 23(12): 2271 - 2273. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. L. Pereira and A. J. Baker A Mitogenomic Timescale for Birds Detects Variable Phylogenetic Rates of Molecular Evolution and Refutes the Standard Molecular Clock Mol. Biol. Evol., September 1, 2006; 23(9): 1731 - 1740. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. I. Stevens, P. Greenslade, I. D. Hogg, and P. Sunnucks Southern Hemisphere Springtails: Could Any Have Survived Glaciation of Antarctica? Mol. Biol. Evol., May 1, 2006; 23(5): 874 - 882. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Galtier, D. Enard, Y. Radondy, E. Bazin, and K. Belkhir Mutation hot spots in mammalian mitochondrial DNA Genome Res., February 1, 2006; 16(2): 215 - 222. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. H. McDonald Apparent Trends of Amino Acid Gain and Loss in Protein Evolution Due to Nearly Neutral Variation Mol. Biol. Evol., February 1, 2006; 23(2): 240 - 244. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Kivisild, P. Shen, D. P. Wall, B. Do, R. Sung, K. Davis, G. Passarino, P. A. Underhill, C. Scharfe, A. Torroni, et al. The Role of Selection in the Evolution of Human Mitochondrial Genomes Genetics, January 1, 2006; 172(1): 373 - 387. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Kumar, A. Filipski, V. Swarna, A. Walker, and S. B. Hedges Placing confidence limits on the molecular age of the human-chimpanzee divergence PNAS, December 27, 2005; 102(52): 18842 - 18847. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Zhang and W.-H. Li Human SNPs Reveal No Evidence of Frequent Positive Selection Mol. Biol. Evol., December 1, 2005; 22(12): 2504 - 2507. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Verginelli, C. Capelli, V. Coia, M. Musiani, M. Falchetti, L. Ottini, R. Palmirotta, A. Tagliacozzo, I. De Grossi Mazzorin, and R. Mariani-Costantini Mitochondrial DNA from Prehistoric Canids Highlights Relationships Between Dogs and South-East European Wolves Mol. Biol. Evol., December 1, 2005; 22(12): 2541 - 2551. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. A. Merriwether, J. A. Hodgson, F. R. Friedlaender, R. Allaby, S. Cerchio, G. Koki, and J. S. Friedlaender Ancient mitochondrial M haplogroups identified in the Southwest Pacific PNAS, September 13, 2005; 102(37): 13034 - 13039. [Abstract] [Full Text] [PDF]
|
|